Abstract
To date, whether and how gene-environment (G × E) interactions operate differently across distinct subtypes of aggression remains untested. More recently, in contrast with the diathesis-stress hypothesis, an alternative hypothesis of differential susceptibility proposes that individuals could be differentially susceptible to environments depending on their genotypes in a “for better and for worse” manner. The current study examined interactions between monoamine oxidase A (MAOA) T941G and catechol-O-methyltransferase (COMT) Val158Met polymorphisms with maternal parenting on two types of aggression: reactive and proactive. Moreover, whether these potential G × E interactions would be consistent with the diathesis-stress versus the differential susceptibility hypothesis was tested. Within the sample of 1399 Chinese Han adolescents (47.2 % girls, M age = 12.32 years, SD = 0.50), MAOA and COMT genes both interacted with positive parenting in their associations with reactive but not proactive aggression. Adolescents with T alleles/TT homozygotes of MAOA gene or Met alleles of COMT gene exhibited more reactive aggression when exposed to low positive parenting, but less reactive aggression when exposed to high positive parenting. These findings provide the first evidence for distinct G × E interaction effects on reactive versus proactive aggression and lend further support for the differential susceptibility hypothesis.
Similar content being viewed by others
References
Albaugh, M. D., Harder, V. S., Althoff, R. R., Rettew, D. C., Ehli, E. A., Lengyel-Nelson, T., & Hudziak, J. J. (2010). COMT Val158Met genotype as a risk factor for problem behaviors in youth. Journal of the American Academy of Child and Adolescent Psychiatry, 49, 841–849. doi:10.1016/j.jaac.2010.05.015.
Anholt, R. R., & Mackay, T. F. (2012). Genetics of aggression. Annual Review of Genetics, 46, 145–164. doi:10.1146/annurev-genet-110711-155514.
Baker, L., Raine, A., Liu, J., & Jacobson, K. C. (2008). Differential genetic and environmental influences on reactive and proactive aggression in children. Journal of Abnormal Child Psychology, 36, 1265–1278. doi:10.1007/s10802-008-9249-1.
Bakermans-Kranenburg, M. J., & van IJzendoorn, M. H. (2011). Differential susceptibility to rearing environment depending on dopamine-related genes: New evidence and a meta-analysis. Development and Psychopathology, 23, 39–52. doi:10.1017/S0954579410000635.
Belsky, J., & Pluess, M. (2009). Beyond diathesis stress: Differential susceptibility to environmental influences. Psychological Bulletin, 135, 885–908. doi:10.1037/a0017376.
Belsky, J., & Pluess, M. (2013). Genetic moderation of early child-care effects on social functioning across childhood: A developmental analysis. Child Development, 84, 1209–1225. doi:10.1111/cdev.12058.
Belsky, J., Pluess, M., & Widaman, K. F. (2013). Confirmatory and competitive evaluation of alternative gene-environment interaction hypotheses. Journal of Child Psychology and Psychiatry, 54, 1135–1143. doi:10.1111/jcpp.12075.
Bongers, I. L., Koot, H. M., Van Der Ende, J., & Verhulst, F. C. (2004). Developmental trajectories of externalizing behaviors in childhood and adolescence. Child Development, 75, 1523–1537. doi:10.1111/j.1467-8624.2004.00755.x.
Brendgen, M., Vitaro, F., Boivin, M., Dionne, G., & Pérusse, D. (2006). Examining genetic and environmental effects on reactive versus proactive aggression. Developmental Psychology, 42, 1299–1312. doi:10.1037/0012-1649.42.6.1299.
Buckholtz, J. W., & Meyer-Lindenberg, A. (2008). MAOA and the neurogenetic architecture of human aggression. Trends in Neurosciences, 31, 120–129. doi:10.1016/j.tins.2007.12.006.
Buil, J. M., Koot, H. M., Olthof, T., Nelson, K. A., & van Lier, P. A. C. (2015). DRD4 genotype and the developmental link of peer social preference with conduct problems and prosocial behavior across ages 9–12 years. Journal of Youth and Adolescence, 44, 1360–1378. doi:10.1007/s10964-015-0289-x.
Burmeister, M., McInnis, M. G., & Zöllner, S. (2008). Psychiatric genetics: Progress amid controversy. Nature Reviews Genetics, 9, 527–540. doi:10.1038/nrg2381.
Caspi, A., McClay, J., Moffitt, T. E., Mill, J., Martin, J., Craig, I. W., & Poulton, R. (2002). Role of genotype in the cycle of violence in maltreated children. Science, 297, 851–854. doi:10.1126/science.1072290.
Chen, X., Liu, M., & Li, D. (2000). Parental warmth, control and indulgence and their relations to adjustment in Chinese children: A longitudinal study. Journal of Family Psychology, 14, 401–419. doi:10.1037/0893-3200.14.3.401.
Chen, X., Wang, L., Chen, H., & Liu, M. (2002). Noncompliance and child-rearing attitudes as predictors of aggressive behaviour: A longitudinal study in Chinese children. International Journal of Behavioral Development, 26, 225–233. doi:10.1080/01650250143000012.
DiLalla, L. F., Bersted, K., & Gheyara, S. J. (2015). Peer victimization and DRD4 genotype influence problem behaviors in young children. Journal of Youth and Adolescence, 44, 1478–1493. doi:10.1007/s10964-015-0282-4.
Dodge, K. A., & Coie, J. D. (1987). Social information processing factors in reactive and proactive aggression in children’s peer groups. Journal of Personality and Social Psychology, 53, 1146–1158. doi:10.1037/0022-3514.53.6.1146.
Drabant, E. M., Hariri, A. R., Meyer-Lindenberg, A., Munoz, K. E., Mattay, V. S., Kolachana, B. S., & Weinberger, D. R. (2006). Catechol O-methyltransferase val158met genotype and neural mechanisms related to affective arousal and regulation. Archives of General Psychiatry, 63, 1396–1406. doi:10.1001/archpsyc.63.12.1396.
Eisenberger, N. I., Way, B. M., Taylor, S. E., Welch, W. T., & Lieberman, M. D. (2007). Understanding genetic risk for aggression: Clues from the brain’s response to social exclusion. Biological Psychiatry, 61, 1100–1108. doi:10.1016/j.biopsych.2006.08.007.
Fan, M., Liu, B., Jiang, T., Jiang, X., Zhao, H., & Zhang, J. (2010). Meta-analysis of the association between the monoamine oxidase-A gene and mood disorders. Psychiatric Genetics, 20, 1–7. doi:10.1097/YPG.0b013e3283351112.
Gershoff, E. T. (2002). Corporal punishment by parents and associated child behaviors and experiences: A meta-analytic and theoretical review. Psychological Bulletin, 128, 539–579. doi:10.1037//0033-2909.128.4.539.
Gohier, B., Senior, C., Radua, J., EI-Hage, W., Reichenberg, A., Proitsi, P., & Surquladze, S. A. (2014). Genetic modulation of the response bias towards facial displays of anger and happiness. European Psychiatry, 29, 197–202. doi:10.1016/j.eurpsy.2013.03.003.
Hartman, S., Widaman, K. F., & Belsky, J. (2015). Genetic moderation of effects of maternal sensitivity on girl’s age of menarche: Replication of the Manuck et al. study. Development and Psychopathology, 27, 747–756. doi:10.1017/S0954579414000856.
Hotamisligil, G. S., & Breakefield, X. O. (1991). Human monoamine oxidase A gene determines levels of enzyme activity. American Journal of Human Genetics, 49, 383–392.
Hubbard, J. A., McAuliffe, M. D., Morrow, M. T., & Romano, L. J. (2010). Reactive and proactive aggression in childhood and adolescence: Precursors, outcomes, processes, experiences, and measurement. Journal of Personality, 78, 95–118. doi:10.1111/j.1467-6494.2009.00610.x.
Kuepper, Y., Grant, P., Wielpuetz, C., & Hennig, J. (2013). MAOA-uVNTR genotype predicts interindividual differences in experimental aggressiveness as a function of the degree of provocation. Behavioural Brain Research, 247, 73–78. doi:10.1016/j.bbr.2013.03.002.
Lachman, H. M., Papolos, D. F., Saito, T., Yu, Y. M., Szumlanski, C. L., & Weinshilboum, R. M. (1996). Human catechol-O-methyltransferase pharmacogenetics: Description of a functional polymorphism and its potential application to neuropsychiatric disorders. Pharmacogenetics, 6, 243–2450. doi:10.1097/00008571-199606000-00007.
Laucht, M., Blomeyer, D., Buchmann, A. F., Treutlein, J., Schmidt, M. H., Esser, G., & Banaschewski, T. (2012). Catechol-O-methyltransferase Val158 Met genotype, parenting practices and adolescent alcohol use: Testing the differential susceptibility hypothesis. Journal of Child Psychology and Psychiatry, 53, 351–359. doi:10.1111/j.1469-7610.2011.02408.x.
Leuchter, A. F., McCracken, J. T., Hunter, A. M., Cook, I. A., & Alpert, J. E. (2009). Monoamine oxidase a and catechol-o-methyltransferase functional polymorphisms and the placebo response in major depressive disorder. Journal of Clinical Psychopharmacology, 29, 372–377. doi:10.1097/JCP.0b013e3181ac4aaf.
Manuck, S. B., Flory, J. D., Ferrell, R. E., Mann, J. J., & Muldoon, M. F. (2000). A regulatory polymorphism of the monoamine oxidase-A gene may be associated with variability in aggression, impulsivity, and central nervous system serotonergic responsivity. Psychiatry Research, 95, 9–23. doi:10.1016/S0165-1781(00)00162-1.
McDermott, R., Tingley, D., Cowden, J., Frazzetto, G., & Johnson, D. D. (2009). Monoamine oxidase A gene (MAOA) predicts behavioral aggression following provocation. Proceedings of the National Academy of Sciences, 106, 2118–2123. doi:10.1073/pnas.0808376106.
Meyer-Lindenberg, A., Buckholtz, J. W., Kolachana, B., Hariri, A. R., Pezawas, L., Blasi, G., & Weinberger, D. R. (2006). Neural mechanisms of genetic risk for impulsivity and violence in humans. Proceedings of the National Academy of Sciences, 103, 6269–6274. doi:10.1073/pnas.0511311103.
Moffitt, T. E. (1993). Adolescence-limited and life-course-persistent antisocial behavior: A developmental taxonomy. Psychological Review, 100, 674–701. doi:10.1037/0033-295X.100.4.674.
Moffitt, T. E. (2005). The new look of behavioral genetics in developmental psychopathology: Gene-environment interplay in antisocial behaviors. Psychological Bulletin, 131, 533–554. doi:10.1037/0033-2909.131.4.533.
Monroe, S. M., & Simons, A. D. (1991). Diathesis-stress theories in the context of life stress research: Implications for the depressive disorders. Psychological Bulletin, 110, 406–425. doi:10.1037//0033-2909.110.3.406.
Munafò, M. R., Durrant, C., Lewis, G., & Flint, J. (2009). Gene × environment interactions at the serotonin transporter locus. Biological Psychiatry, 65, 211–219. doi:10.1016/j.biopsych.2008.06.009.
Odgers, C. L., Moffitt, T. E., Broadbent, J. M., Dickson, N., Hancox, R. J., Harrington, H., & Caspi, A. (2008). Female and male antisocial trajectories: From childhood origins to adult outcomes. Development and Psychopathology, 20, 673–716. doi:10.1017/S0954579408000333.
Pettit, G. S., Bates, J. E., & Dodge, K. A. (1997). Supportive parenting, ecological context, and children’s adjustment: A seven-year longitudinal study. Child Development, 68, 908–923. doi:10.1111/j.1467-8624.1997.tb01970.x.
Pickles, A., Hill, J., Breen, G., Quinn, J., Abbott, K., Jones, H., & Sharp, H. (2013). Evidence for interplay between genes and parenting on infant temperament in the first year of life: Monoamine oxidase A polymorphism moderates effects of maternal sensitivity on infant anger proneness. Journal of Child Psychology and Psychiatry, 54, 1308–1317. doi:10.1111/jcpp.12081.
Pluess, M., & Belsky, J. (2013). Vantage sensitivity: Individual differences in response to positive experiences. Psychological Bulletin, 139, 901–916. doi:10.1037/a0030196.
Smolka, M. N., Schumann, G., Wrase, J., Grusser, S. M., Flor, H., Mann, K., & Heinz, A. (2005). Catechol-O-methyltransferase val158met genotype affects processing of emotional stimuli in the amygdala and prefrontal cortex. Journal of Neuroscience, 25, 836–842. doi:10.1523/JNEUROSCI.1792-04.2005.
Substance Abuse and Mental Health Services Administration (SAMHSA). (2014). Results from the 2013 national survey on drug use and the health: Summary of national findings (Office of Applied Studies, NSDUH Series H-48, HHS Publication No. SMA 14-4683). Rockville, MD: SAMHSA.
Tadić, A., Müller, M. J., Rujescu, D., Kohnen, R., Stassen, H. H., Dahmen, N., & Szegedi, A. (2007). The MAOA T941G polymorphism and short-term treatment response to mirtazapine and paroxetine in major depression. American Journal of Medical Genetics Part B: Neuropsychiatric Genetics, 144, 325–331. doi:10.1002/ajmg.b.30462.
Thompson, J. M., Sonuga-Barke, E. J., Morgan, A. R., Cornforth, C. M., Turic, D., Ferguson, L. R., & Waldie, K. E. (2012). The catechol-O-methyltransferase (COMT) Val158Met polymorphism moderates the effect of antenatal stress on childhood behavioural problems: Longitudinal evidence across multiple ages. Developmental Medicine and Child Neurology, 52, 148–154. doi:10.1111/j.1469-8749.2011.04129.x.
Tremblay, R. E. (2010). Developmental origins of disruptive behaviour problems: The ‘original sin’ hypothesis, epigenetics and their consequences for prevention. Journal of Child Psychology and Psychiatry, 51, 341–367. doi:10.1111/j.1469-7610.2010.02211.x.
Tuvblad, C., Raine, A., Zheng, M., & Baker, L. A. (2009). Genetic and environmental stability differs in reactive and proactive aggression. Aggressive Behavior, 35, 437–452. doi:10.1002/ab.20319.
van Ijzendoorn, M. H., Caspers, K., Bakermans-Kranenburg, M. J., Beach, S. R., & Philibert, R. (2010). Methylation matters: Interaction between methylation density and serotonin transporter genotype predicts unresolved loss or trauma. Biological Psychiatry, 68, 405–407. doi:10.1016/j.biopsych.2010.05.008.
Verma, D., Chakraborti, B., Karmakar, A., Bandyopadhyay, T., Singh, A. S., Sinha, S., & Rajamma, U. (2014). Sexual dimorphic effect in the genetic association of monoamine oxidase A (MAOA) makers with autism spectrum disorder. Progress in Neuro-Psychopharmacology and Biological Psychiatry, 50, 11–20. doi:10.1016/j.pnpbp.2013.11.010.
Volavka, J. A. N., Bilder, R., & Nolan, K. (2004). Catecholamines and aggression: The role of COMT and MAO polymorphisms. Annals of the New York Academy of Sciences, 1036, 393–398. doi:10.1196/annals.1330.023.
Wakschlag, L. S., Kistner, E. O., Pine, D. S., Biesecker, G., Pickett, K. E., Skol, A., & Cook, E. H. (2010). Interaction of prenatal exposure to cigarettes and MAOA genotype in pathways to youth antisocial behavior. Molecular Psychiatry, 15, 928–937. doi:10.1038/mp.2009.22.
Wang, F. M., Chen, J. Q., Xiao, W. Q., Ma, Y. T., & Zhang, M. (2012). Peer physical aggression and its association with aggressive beliefs, empathy, self-control, and cooperation skills among students in a rural town of china. Journal of Interpersonal Violence, 27, 3252–3267. doi:10.1177/0886260512441256.
Widaman, K. F., Helm, J. L., Castro-Schilo, L., Pluess, M., Stallings, M., & Belsky, J. (2012). Distinguishing ordinal and disordinal interactions. Psychological Methods, 17, 615–622. doi:10.1037/a0030003.
Widom, C. S., & Brzustowicz, L. M. (2006). MAOA and the “cycle of violence”: Childhood abuse and neglect, MAOA genotype, and risk for violent and antisocial behavior. Biological Psychiatry, 60, 684–689. doi:10.1016/j.biopsych.2006.03.039.
Williams, L. M., Gatt, J. M., Grieve, S. M., Dobson-Stone, C., Paul, R. H., Gordon, E., & Schofield, P. R. (2010). COMT Val 108/158 Met polymorphism effects on emotional brain function and negativity bias. Neuroimage, 53, 918–925. doi:10.1016/j.neuroimage.2010.01.084.
Windhorst, D. A., Mileva-Seitz, V. R., Linting, M., Hofman, A., Jaddoe, V. W., Verhulst, F. C., & Bakermans-Kranenburg, M. J. (2015). Differential susceptibility in a developmental perspective: DRD4 and maternal sensitivity predicting externalizing behavior. Developmental Psychobiology, 57, 35–49. doi:10.1002/dev.21257.
Zhang, W., Cao, Y., Wang, M., Ji, L., Chen, L., & Deater-Deckard, K. (2015). The dopamine D2 receptor polymorphism (DRD2 TaqIA) interacts with maternal parenting in predicting early adolescent depressive symptoms: Evidence of different susceptibility and age differences. Journal of Youth and Adolescence, 44, 1428–1440. doi:10.1007/s10964-015-0297-x.
Acknowledgments
This study was supported by the National Natural Science Foundation of China (31271105), the Specialized Research Fund for the Doctoral Program of Higher Education (20133704110001) and the Natural Science Foundation of Shandong Province (ZR2014CQ030).
Author Contributions
WZ conceived of the study, participated in its design and coordination and drafted the manuscript; CC participated in its design, performed the statistical analysis and drafted the manuscript; MW participated in the design and helped to draft the manuscript; LJ helped to draft the manuscript; YC helped to draft the manuscript. All authors read and approved the final manuscript.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
All authors declare no conflicts of interest.
Ethical Approval
All procedures followed were in accordance with the ethical standards of the ethics committee on human experimentation of Shandong Normal University and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.
Informed Consent
Informed assent (adolescents) and consent (mothers, teachers and school principals) were obtained from all participants for being included in the study.
Rights and permissions
About this article
Cite this article
Zhang, W., Cao, C., Wang, M. et al. Monoamine Oxidase A (MAOA) and Catechol-O-Methyltransferase (COMT) Gene Polymorphisms Interact with Maternal Parenting in Association with Adolescent Reactive Aggression but not Proactive Aggression: Evidence of Differential Susceptibility. J Youth Adolescence 45, 812–829 (2016). https://doi.org/10.1007/s10964-016-0442-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10964-016-0442-1